Traumatic lung

Forensic Science Elsevier Sequoia S.A., Lausanne

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in The Netherlands

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IAN WEBSTER and LRILA JOAN BLUM National Research Institute for Occupational Diseases, S.A. Medical Research (South Africa)

Council, Johannesburg

SUMMARY

Injuries to the lung can be due to many causes such as blast injury, fat embolism or injury to the thoracic cage. The term “traumatic lung” refers to changes in the lung which

occur in trauma elsewhere in the body such as head injuries or associated with shock. The lung parenchyma can show oedema, haemorrhage or desquamative alveolitis or a combination of any of these. Electron microscopy may show granularity of the endothelial cells of the capillary with widening of the canal between the cells. There may also be oedema of the basement membrane and degenerative changes in the alveolar epithelium followed by swelling and desquamation. From the medicolegal aspect it is not possible to state that trauma can be the sole cause of these changes as a similar picture can be produced by other conditions such as oxygen toxicity, viral infections and toxins, and a full clinical history is important

in diagnosis.

There are many problems associated with the pathology important

problems

an unequivocal

are: a. Is traumatic

lung an entity

of traumatic

lung. Two of the

on which the pathologist

can give

and b. Are the basic pathological changes common to a number and is it possible to exclude the other causes of the pathological

opinion,

of other conditions

changes. The answers to these problems affect not only the assessment of the relationship of lung changes to the cause of death, but the liability treatment

for pulmonary

disability

and

should the injured party survive.

It is undoubted

that not only do lung changes occur when the thoracic cage is injured

but severe lung changes can be found following trauma to any part of the body. In order to understand the nature of traumatic lung, it is necessary to review what is known of the structure of the lower respiratory tract. The respiratory tract can be divided into 2 zones, namely the conducting system and the respiratory part of the lung. Through the trachea, bronchi and large bronchioles, air is conveyed to the respiratory portion (Fig. 1) where, in the finer ramifications and terminal alveoli, gases are transferred to and from the blood capillaries in the alveolar walls (Fig. 2). There is a reduction in the thickness of the walls of the structures of the lower respiratory tract which eventually consist of alveolar epithelial cells, connective tissue elements and the wall of the capillary. Forens. Sci., 1 (1972)

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168

Fig. 1. Diagrammatic representation of the lower bronchioles first-, second- and third-order.

I. WEBSTER,

respiratory

tract.

L.J. BLUM

RBL, RB2 and RB3, respiratory

It was only when the magnifying powers of the electron microscope became available that the details of the alveolar capillary barrier became known and the somewhat complex mechanism of gas transfer better understood. The ultrastructure of the alveolar wall is that of the endothelial cell of the capillary, the basement membrane and the different types of alveolar epithelial cells. Important in our understanding of the pathology of the traumatic lung is that between the adjacent endothelial cells is a canal by which the lumen of the capillary connects to the basement membrane and eventually to the alveolar space (Fig. 3). Many factors cause changes in these endothelial cells, resulting in swelling

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Fig. 2. Ultrastructure canal (Magnification: ALV, alveolar space.

and consequently

of the capillary 54 000X; inset,

widening

endothelium showing the gas transfer vesicles and intercellular 14 000X). CAP, capillary; END, endothelial cell; V, vesicles;

of these canals, sometimes to such an extent that the cellular

elements of the blood can pass through. When morphometrists and physicists

examined

the lung, it was found that the shape

of an alveolus would evolve a surface tension of approximately 35 dynes per sq cm in the alveolar lumen. As the tension in the capillaries is in the region of 15 dynes per sq cm; the alveolus should have a high attracting force on the blood plasma and cellular constituents. These would then be drawn into the alveoli which would collapse. It is now known that there is a layer of low surface tension material (known as “surfactant”) lining the alveolar walls which neutralizes the surface tension inherent in the shape of the alveolus. This Forens.

Sci,

1(1972)

167 - 178

170

Fig. 3.

I. WEBSTER,

L.J. BLUM

of the alveolar wall. (Magnification: 54 000x). CAP, capillary; END, capillary membrane; EP, alveolar epithelium; AL, alveolar lining. The basement is oedematous and the endothelial and epithelial cells are more granular than usual. The and non-osmophilic layers of the alveolar lining are shown.

Ultrastructure

endothelial cell; BM, basement membrane osmophilic

material

is secreted

by cells lining the alveolus,

the granular pneumocytes,

but this se-

cretion also depends on the pulmonary capillary pressure (Fig. 4). The alveolar lining consists of 2 fractions’, a base layer containing proteins and mucopolysaccharides, and a lamellar superficial layer consisting of polar lipids and water. The lining substance is found in the pores of Kohn and the canals of Lambert and is presumably circulating. Not only does this fluid prevent adhesiveness but it is in this circulating fluid that the macrophages or defence cells of the lung are moved to the respiratory bronchioles. The importance of the fluid membrane of the alveoli is that it indicates that there is a continual movement of the blood plasma into the alveolar spaces. The control of the

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Fig. 4. Diagrammatic representation the relative pressures in the capillary

amount follows:

of this fluid depends

of the alveolar wall. The figures 15 dynes and 40 dynes refer to and the alveolar space should the surfactant lining be absent.

on a number

of factors which may be summarized

as

1. The integrity of the capillary endothelium. If this is damaged fluid escapes and lifts the lining of the alveolar epithelial cells. Thus more fluid will escape and block the pores of Kohn and canals of Lambert. 2. The degree of patency of the endothelial cell canals. If these become wider more fluid will escape and there will be a similar effect. 3. The state of the basement membrane. If it becomes collagenized

it will be difficult for

the fluid to pass through. 4. The type and number of the alveolar epithelial cells. In certain conditions, e.g. inhalation of nitrous oxide, the granular pneumocytes are affected and only membranous pneumocytes line the alveoli so that no surfactant is produced. 5. The effectiveness of the surfactant lining. If there is any suprarenal damage then surfactant production is reduced. The secretion of surfactant also depends on the pulmonary capillary blood pressure and if this is too low then surfactant is not secreted. 6. Blood flow through the lung.

Forens.

Sci,

l(1972)

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I. WEBSTER, L.J. BLUM

Although associated

the term “traumatic

with a particular

the respiratory

lung” is commonly used to indicate pulmonary lesions

biochemical

change in the metabolism

of an injured person,

tract may be affected by trauma in a number of different

was the lung involved in patients with haemorrhagic

ways. So often

shock that Sealy and his co-workers3

considered that the lung was the target organ in the state of shock. Grant and Reeve4 stated in 195 1 that of all the organs the lungs were most frequently abnormal at autopsy. They were most concerned with the pathology of fat embolism but according to Simeone’ some of their patients could have shown other effects of trauma of the lung. That the lung could be the target organ of the “shock state” becomes evident from the descriptions

of the different

changes which can occur in the lung. However, there are two

main factors which cause the lung to be the target organ. Firstly,

the lung has a poorly

supported

vascular system and any capillary damage is more easily seen. Secondly, the studies of Hardaway ” indicate that haemorrhage and shock are associated with intravascular coagulation, which is facilitated by the lower pressures of the pulmonary circula-

tion. In pathological conditions of the lung which are very similar to the “shocked lung” not only is the lung the target organ but the endothelial cells of the capillaries of the lung are the target cells for a number of disease states and toxic reactions including shock and trauma. INJURY OF THE THORACIC

CAGE

That the lung will be damaged in direct or crush injuries to the chest is easily understood, but very often the changes in the lung are more extensive for by haemorrhage

from the injured lung. In addition

than can be accounted

to haemorrhage,

oedema of the

alveolar spaces is found. This is caused by alteration of the blood flow through certain parts of the lung, increase of capillary pressure due to capillary constriction or by intravascular coagulation Swank

of the blood elements.

and his colleagues6

suggested that in severe trauma there is an increase of 5hydroxytryptamine (serotonin) or its metabolites and that the aggregation of the blood elements is increased by small amounts of adenosine phosphate. Aggregation of these blood elements is found 15 minutes after trauma. They demonstrated that radioactive S-hydroxytryptamine was trapped in the lung. It has been shown in our unit that if silica shock is induced by the intravenous inoculation of fine silica particles the animal dies in a few seconds. In these cases an increase in circuiating 5hydroxytryptamine was found. BLAST INJURIES

The blast of high explosives may cause haemorrhagic lesions in various internal organs, including the lungs, without there being any evidence of external injury7. This was considered to be due to lowering of the alveolar pressure by the sudden reduction of pressure of the suction wave of the blast’, or by the distension of the lungs because of the sudden pressure increase. However, the experimental evidence of Zuckerman’ in

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173

1940 showed conclusively chest wall because

that blast injuries

animals

clothed

were caused by the pressure wave on the

with thick layers

of rubber

suffered

little or no

damage. FAT EMBOLI

Following

trauma,

emboli

may be found

in the circulating

blood

and may be of

different types such as fat, fibrin or fragments of tissue. Of these the most common are fat emboli, usually associated with fractured bones, trauma of fatty connective tissue ortrauma of the liver when there is marked fatty change in that organ’ ‘. The pathology found in fat embolisation of the lung has always been difficult explain.

It was thought

emboli. It appears, fracture site, and it the features of fat from the fat cause

that changes were produced

by obstruction

however, that more fat is present than could be produced from a has also been found that fat injected intravenously does not produce embolism. What probably does occur is that the fatty acids derived damage to the endothelial cells and this causes the oedema and

haemorrhage into the alveolar spaces” I. An interesting observation was made by Kent 12 in a series of 53 diabetic patients. 24 patients,

number,

In

fat emboli were found in the lungs at autopsy and of these, 3 showed emboli

in almost every field examined under the microscope. from trauma

to

of the capillaries by

within

3 weeks of death.

11 showed occasional

None of these patients had suffered

Of a non-diabetic

control

fat emboli only. It therefore

series of the same

appears that although

fat

emboli can occur to a marked degree, they may cause no effect. CONGESTIVE

ATELECTASIS

In any review of the literature on the effects of trauma on the lung, the term congestive atelectasis is often found. This is a descriptive term for areas of congestion and haemorrhage

which give the lung a solid appearance.

The use of this term probably

follows on the work of de Takats and his co-workers1 3, who found that after trauma there was a decided contraction of the bronchial tree with constriction which was accompanied by an increase of the secretions into the bronchial tree. Unfortunately the plates of the angiograms in de Takats’ article have not reproduced well and it is difficult to confirm the finding of constriction on the evidence given. Should such circumstances arise, however, retention of secretion in the constricted bronchial tree would lead to obstruction and therefore collapse of parts of the lung. If the obstructed bronchus were of major size then massive collapse or atelectasis would occur. Most of the work done by de Takats was on pulmonary emboli and there is some doubt as to whether such vascular emboli will cause bronchial or even arterial constriction. POST-PERFUSION

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It is reasonable to expect that if the circulation is overloaded with fluids as might occur with intravenous therapy, transudation of fluid will occur and the fluid will escape Forem. Sci., l(1972)

167 - 178

174

I. WEBSTER,

from the capillaries into the alveolar spaces. Such transudation the walls of the lower respiratory pulmonary

oedema

is more likely to occur if

tract are damaged either by disease or trauma, and the

may be well marked.

where the cardiorespiratory

L.J. BLUM

Since the introduction

organs are by-passed

of open heart surgery

wholly or partially for as long as 3 or 4

hours, the so-called “pump lung” may be found. A haemorrhagic oedema and atelectasis develop which do not depend on whether the circuit was primed with homologous or autologous blood’ 4 or dextran. The lesions are similar to those found in hypovolaemic shock and result from anoxia, hypotension, foreign proteins or denaturation of blood elements by the oxygenation system in use. It is considered that these factors will cause haemorrhagic oedema through their effect on the target cell - the capillary endothelium. There are many conditions which may be associated with, or may be confused with, what is known as traumatic lung. Although this pathology is most often found after severe nonthoracic

following burns, after cardiac surgery and described the autopsy findings of 100 in endotoxic shock. Martin and his colleagues” patients who died of shock in the United States Army either in the home country or in Vietnam. patient metabolic

trauma,

it has also been described

The relationship with

an unstable

of the development blood

volume

of traumatic

was suggested

changes associated with the development

in the experiments

carried

out

lung to fluid overload in a

by Gomez’ 6. The different

of traumatic

by Henry’ 7 -r 9. Simeone’

lung are well described quotes

Hardaway,

who

described a new type of surgical patient in Vietnam and pointed out the occurrence of severe acidosis or alkalosis in some of the cases where pulmonary changes occurred. Simeone also contends that some of the cases described by Reeve in 195 1 may have been similar to those described in Vietnam. Following trauma the lung parenchyma may show one or all of the following changes: 1. The lower respiratory tract may be filled with oedematous fluid. This is known as the wet lung, traumatic lung, or pump lung. 2. Haemorrhage, in which the alveolar spaces are filled with red blood cells. 3. Desquamative alveolitis, in which the alveolar epithelial cells become swollen following oedema of the basement membrane of the alveolar wall. The swollen alveolar epithelial cells are then shed into the alveolar spaces (Fig. 5). This is one type of lung change, the dry lung, found in the Vietnam casualties which were flown from the battle area to the base hospital as rapidly as possible. In this way it was possible to exclude a number of factors which could have caused such a lesion. The fundamental changes in both the wet traumatic lung and the desquamative alveolitis are the same, namely a granularity of the endothelial cell of the capillary followed a widening of the canals between the endothelial cells. The plasma may then pass into basement membrane and eventually into the alveolar spaces. With the oedema of basement membrane degenerative changes develop in the alveolar epithelium resulting

by the the in

swelling of these cells and subsequent desquamation which may be such as to fill the alveolar spaces. This interferes with the normal alveolar fluid circulation as the circulating canals become blocked, and with the degeneration of one type of epithelial cell there is diminished secretion of surfactant.

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Fig. 5. Section cells (200X).

of lung one week

after

trauma

showing

the desquamation

of the alveolar

epithelial

It is not yet clear why in some cases there is oedema whilst in others a desquamation of cells takes place. It may well be that these are evidence of different degrees of severity of the shock state of the lung, in which case an admixture

of the 2 lesions would be

expected. This indeed does occur and often there is diapedesis of the red cells through the canals into the alveolar spaces giving the appearance of haemorrhage into the alveoli. In some instances the oedematous fluid and fibrin components are compacted by air against the alveolar walls to form hyaline membranes.

The presence of these membranes

is often

associated with a lack or deficiency of the low-surface-tension lining of the alveoli. From the medicolegal aspects it would have been a matter of much importance were it possible to state that shock was the only cause of such a pathological pattern. Not only do other factors affect the endothelial cells and the alveolar cells producing an identical pathological picture, but these other factors may act to enhance the degree of the pathology produced by shock. Forens.

Sci., 1 (1972)

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176

The administration

I.WEBSTER,

of oxygen,

especially

of more than

1 atmosphere

L.J. BLUM

and at high

concentration produces almost identical changes (Fig. 6). These changes probably first appear about 6 hours after commencing administration of oxygen resuscitation therapy. Toxin, particularly

from Gram negative bacilli, and possibly from cocci, may damage

the endothelial cells. Here the damage may be related to the aggregation of ferritin as occurs in Type I sensitivity reactions in the lung. The pathological changes in the lung in endotoxic shock are almost identical to those found in trauma. One of the major difficulties in reaching a diagnosis of a shock lung is to exclude a concomitant viral infection which will produce desquamation cells, interstitial oedema and haemorrhage. Using electron possible to distinguish

a viral pneumonitis

Fig. 6. Section of lung after prolonged of epithelial cells. (320x).

oxygen

of the alveolar epithelial microscopy it should be

from a shock lung, but the medicolegal

therapy

showing

interstitial

fibrosis

formali-

and desquamation

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ties which are necessary tissue sufficiently

before an autopsy

can be performed

examination, or by culture methods. Should the patient recover, the pathological provided

the extent

circulatory

preclude

taking the lung

soon after death to establish the diagnosis by electron

of interstitial

pathways

changes of traumatic

lung may resolve

oedema has not been too great. Bearing in mind the

of the alveolar fluid, should the interstitial

or canals, the fluid or the desquamative this occur for any length

microscopical

of time connective

between the cells causing organisation

oedema block the pores

cells will remain in the alveolar spaces, and should tissue fibrils will grow into the fluid or

of the alveolar spaces.

In order to establish the exact nature of the lesion produced in the lungs after trauma, all of the modern

techniques,

including

this way that some of the conditions clinical

condition

combining

As with other pulmonary on such a specimen

microscopy

should be used. It is only in the pathological

lung may be assessed. Others

what is seen macroscopically

the patient. to report

of the shocked

electron

which may enhance and microscopically pathology,

without

referring party not to provide the pathologist

by

with the clinical history

while it is immoral

the clinical history,

features and

can be excluded

of

for the pathologist

it is almost criminal

for the

with all the available details.

REFERENCES 1

2

E.R. Weibel and _I. Gil, Electron microscope alveoli, Respir. Physiol., 4 (1968) 42-57. M.W. Larnbert, Accessory bronchiole-alveolar

demonstration

of extracellular

communications,

duplex

lining layer of

J. Puthol. Bucteriol.,

70 (1955)

311-314. 3

W.C. Scaly, S. Ogino, A.M. Lesage and W.G. Young,

4

in hemorrhagic shock, Surg. Gynecol. Obstet., 122 (1966) 154-760. R.I. Grant and E.B. Reeve, Observations on the General Effects of Injury in Man, H.M.S.O., London, 195 1, p. 313. (Medical Research Council special report no. 277).

5 6 I 8 9 10

11 12 13 14 15

Functional

and structural

changes

in the lung

F.A. Simeone, Pulmonary complications of nonthoracic wounds: A historical perspective, J. Trauma, 8 (1968) 625-648. R.L. Swank, W. Hissen and SE. Bergen&, 5-Hydroxytryptamine and aggregation of blood eicments after trauma, Surg. Gynecol. Obstet., 119 (1964) 7799784. D.D. Logan, Detonation of high explosive in shell and bomb, and its effects, Br. Med. J., 2 (1939) 816 and 864. S. Zuckerman, Discussion on problems of blast injuries, Proc. Roy. Sot. Med., 34 (1941) 171-192. S. Zuckerman, Experimental study of blast injuries to W.S. Hartcroft and J.H. Ridout, Pathogenesis of the Escape of lipid from fatty hepatic cysts into biliary (1951) 951-989. L.F. Peltier, Fat embolism; toxic properties of neutral

the lungs, Lancet, 2 (1940) 219-224. cirrhosis produced by choline deficiency: and vascular systems, Am. J. Pathol.: 27 fat and free fatty

acids, Surgery, 40 (1956)

665-170. S.P. Kent, Fat embolism in diabetic patients without physical trauma, Am. J. PafhoZ.,31 (1955) 339-403. G. de Takats, G.K. Fenn and E.L. Jenkinson, Reflex pulmonary atelectasis, J. Am. Med. Assoc., 120 (1942) 686-690. R. Schramel, F. Schmidt, F. Davis, D. Palmisano and 0. Creech, Pulmonary lesions produced by prolonged perfusion, Surgery, 54 (1963) 224-231. A.M. Martin, H.B. Soloway and R.L. Simmons, Pathologic anatomy of the lungs following shock

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19 20

1. WEBSTER,

L.J. RLUM

and trauma, J. Trauma, 8 (1968) 687-698. A.C. Gomez, Pulmonary insufficiency in nonthoracic trauma, J. Trauma, 8 (1968) 656-675. J.N. Henry, The effect of shock on pulmonary alveolar surfactant, J. Trauma, 8 (1968) 756-770. J.N. Henry, A.H. McArdle, G. Bounous, L.G. Hampen, H.J. Scott and F.N. Gund,The effect of experimental hemorrhagic shock on pulmonary alveolar surfactant, 1 Trauma, 7 (1967) 691-726. J.N. Henry, A.H. McArdle, H.J. Scott and F.N. Gund, A study of the acute and chronic respiratory pathophysiology of hemorrhagic shock, J. Tkorac. Curdiovasc. Surg., 54 (1967) 666-681. R.M. Hardaway, The role of intravascular clotting in the etiology of shock, Ann. Surg., 155 (1962) 3522338.